Evolution in Action . Matthias Glaubrecht Editor IncooperationwithHaraldSchneider Evolution in Action Case studies in Adaptive Radiation, Speciation and the Origin of Biodiversity SpecialvolumeoriginatingfromcontributionstothePriorityProgramme SPP1127“Radiations:OriginsofBiologicalDiversity”oftheDeutsche Forschungsgemeinschaft Dr.MatthiasGlaubrecht Museumfu¨rNaturkundeBerlin LeibnitzInstituteforResearchin EvolutionandBiodiversityatthe HumboldtUniversity Invalidenstraße43 10115Berlin Germany [email protected] Incooperationwith Dr.HaraldSchneider DepartmentofBotany NaturalHistoryMuseum London ISBN978-3-642-12424-2 e-ISBN978-3-642-12425-9 DOI10.1007/978-3-642-12425-9 SpringerHeidelbergDordrechtLondonNewYork LibraryofCongressControlNumber:2010930166 # Springer-VerlagBerlinHeidelberg2010 Thisworkissubjecttocopyright.Allrightsarereserved,whetherthewholeorpartofthematerialis concerned,specificallytherightsoftranslation,reprinting,reuseofillustrations,recitation,broadcasting, reproductiononmicrofilmorinanyotherway,andstorageindatabanks.Duplicationofthispublication orpartsthereofispermittedonlyundertheprovisionsoftheGermanCopyrightLawofSeptember9, 1965,initscurrentversion,andpermissionforusemustalwaysbeobtainedfromSpringer.Violations areliabletoprosecutionundertheGermanCopyrightLaw. Theuseofgeneraldescriptivenames,registerednames,trademarks,etc.inthispublicationdoesnotimply, evenintheabsenceofaspecificstatement,thatsuchnamesareexemptfromtherelevantprotective lawsandregulationsandthereforefreeforgeneraluse. Coverillustration: Top:Typicalmoundoftermitesspecies(Macrotermesmichaelseni)atKajiado,Kenya(fromMarten etal.,thisvolume;photography:ManfredKaib). Left:Wildtomatoes(Solanum sect.Lycopersicon):S.chilensefromtheMoqueguapopulation,Peru (fromStephan&Sta¨dler,thisvolume;photography:GabrielClostre). Middle:NewandsofarundescribedfreshwatergastropodspeciesofTylomelaniafromLakePosoon Sulawesi,Indonesia(fromRintelenetal.,thisvolume;photography:ChrisLukhaup). Right:OrchidOphryssphegodeswithpseudocopulatingmalesofthepollinatorAndrenanigroaenea (fromAyasseetal.,thisvolume;photography:ManfredAyasse). Coverdesign:WMXDesignGmbH,Heidelberg,Germany Printedonacid-freepaper SpringerispartofSpringerScience+BusinessMedia(www.springer.com) Preface Radiations, or Evolution in Action We have just celebrated the “Darwin Year” with the double anniversary of his 200th birthday and 150th year of his masterpiece, “On the Origin of Species by meansofNaturalSelection”.Inthiswork,Darwinestablishedthefactualevidence ofbiologicalevolution,thatspecieschangeovertime,andthatneworganismsarise bythesplittingofancestralformsintotwoormoredescendantspecies.However, above all, Darwin provided the mechanisms by arguing convincingly that it is by naturalselection–aswellasbysexualselection(ashelateradded)–thatorganisms adapt to their environment. The many discoveries since then have essentially confirmed and strengthened Darwin’s central theses, with latest evidence, for example, from molecular genetics, revealing the evolutionary relationships of all lifeformsthroughonesharedhistoryofdescentfromacommonancestor.Wehave also come a long way to progressively understand more on how new species actually originate, i.e. on speciation which remained Darwin’s “mystery of mys- teries”,asnotedinoneofhisearliesttransmutationnotebooks.Sincespeciationis the underlying mechanism for radiations, it is the ultimate causation for the biologicaldiversityoflifethatsurroundsus. Aswehavelearned,atthelatestduringlastyear’scelebrationofCharlesDarwin andhisdiscoveryofevolution,itwasnotonlytheimmediatenaturalobjectsfrom the “Beagle’s” circumnavigation of the globe 1831–1836 that Darwin observed, collected and reported on that provided him with basal evidence for organic evolution.Evenmoreimportantwas hissecond,longer journeytodiscoveryafter hisreturntoEngland,whenDarwindevelopedhis“theorytoworkwith”,asheonce wrote, after thinking about the Malthusian paradigm of the enormous fertility of organisms that surpassed the capacity of available resources. It was only through thissecondvoyageduringmorethantwodecades,fromearly1837tohisepochal publication in 1859 when Darwin patiently and dedicatedly substantiated his theory, that he truly completed the “Copernican Revolution” in biology. That wayhefinallybrought“theoriginandadaptationsoforganismsintheirprofusion and wondrous variation into the realm of science”, as Ayala and Avise recently pointedout(ProcNatlAcadSciUSA,106(2009):2475–2476). v vi Preface Aroundtheglobe,wehavein2009commemoratedtwocenturiesofDarwinwith numerous colloquia, conferences, cloud-gathering festivals, and museum exhibi- tions, and with new books and research articles in journals. The research papers compiled in the present volume also reveal some of the many aspects among the widespectrumofcurrentapproachesinevolutionaryresearch,followinglargelyin Darwin’sfootsteps.Inmanyways,wetodaystillrelatetotheplethoraofobserva- tionsandnotesDarwinmademorethanacenturyago.Ontheotherhand,wehave the privilege to use modern techniques, for example, from molecular biology and from systematic phylogeny, to allow the reconstructing of the relationships of organisms and the course of evolution – an accumulation of knowledge Darwin couldnothaveimaginedbutthathecertainlywouldhavelovedtoknowabout. Beyonddoubt,CharlesDarwin’scontributiontoourunderstandingoftheorigin ofbiodiversitycannotbeoverestimated,asaverynaturaltransitionwillleadfrom theDarwinYearto2010astheYearofBiodiversityandConservation.Thisbookis a contribution to both celebrations, with the studies and model cases presented showingtheprogressanddynamicofresearchbasedonDarwiniantheoriesaswell assheddinglightontheimplicationsincontextwiththecurrentbiodiversitycrises. Thegreatimportanceofadaptive(andnon-adaptive)radiationsfor biodiversityis widelyaccepted,butourunderstandingoftheprocessesandmechanismsinvolved is still limited, and generalizations need to be based on the accumulation of more evidencefromadditionalcasestudies.Ourmodelcasesare,moreoftenthannot,in need of being conserved, with their immediate habitats where we find and study thembeingbetterprotected. The studies presented in this volume are those urgently needed case studies focusing on a variety of organisms and different aspects of radiations. As case studies in evolution, they are also taking advantage of the progress in molecular biology and bioinformatics, two areas that have revolutionized modern biology. Thescientificresultspresentedhereinareexcellentexamplesnotonlyofevolution in action, but also of active research on evolutionary processes and their most apparentoutcome,viz.thebiodiversitythatwewanttoconserveforfuturegenera- tionstoenjoy. This volume aims at bringing together the immediate results of studies and projects conducted within a priority programme funded by the Deutsche For- schungsgemeinschaft(DFG)from2002to2008(seemoreonthisinthefollowing introductorychapterbyBillMartin).Here,theinsightsof25researchgroupswitha totalof109contributorsarearrangedinthreeparts:Thefirstpart(1)isconcerned with approaches in botany (8 papers), the second part (2) with host-plant interac- tions(4papers),andthethirdpart(3)withapproachesinzoology(13papers);all summarizingtheadvanceswehavemadesofar. Theauthorswereaskedtopresenttheirresearchwithscientificrigor,albeitnot necessarilypresenting itintheusualformofaresearchpaper,butifpossibleasa morereadablereview.Thatway,wehavehopedtonotsomuchwriteonlyforthe few other experts in our immediate field of expertise (be it Solanum genetics, Crematogaster ants on Malaysian Macaranga plants, or Tylomelania snails in lakesonSulawesi),butforawideraudience.Atthesametime,wehopetopresent Preface vii here a colorfully illustrated survey of current evolutionary biology research in Germany.Thesepapersorchapters,althoughtheywereallindependentlywritten, areheregroupedaccordingtotheirmainsubjects,theirhypothesestested,andtheir major findings and implications. Of course, other arrangements are also possible; however, the present compilation follows an inherent design suggested by their contentsthatIwillbrieflyoutlinehere. Starting with model cases for radiations in ferns on Madagascar (Schneider etal.),inplantsonMacaronesianislands(Thivetal.)andHordeumintheAmericas (Blattner et al.), a main underlying theme in this book will be the question of the drivingforcesresponsibleforspeciesevolution.Thisisdiscussed,forexample,for keyinnovationsforferns(Schneideretal.),thematingsysteminCapsella(Paetsch etal.)and,inparticular,forecologicalfactors–thelatteractuallybeingthemajor recurrentfactorinfocusinmanyofthepaperscompiledhere–suchaspollinator- drivenspeciationinorchids(Ayasseetal.).Thebotanysectionconcludeswithtwo papers looking into population genetics and genetic diversity in plants used for humanfood,suchastomatoes(Stephanetal.)andwheatandbarley(Kilianetal.). InpartII,fourpaperslookatcasestudiesinhost–plantinteractionsasaspecial caseofbioticevolution,searchingforgeneralprinciplesthatapplytothoseanimals thatdirectly liveon,inorwith plantsand viceversa.The paperby Weising et al. discusses Macaranga speciation, the paper by Feldhaar et al. on speciation in Crematogaster adds the ant perspective to the story. Another intriguing case study on plants comes from the plethora of forms in wild roses interacting with fungi and insects (Kohnen et al.), while Johanneson et al. follow the traces of speciationinplant-dwellingtephritidflies. PartIIIonthezoologicalapproachesstartswithexaminingradiationsagainand some of the proposed key factors responsible for diversification and speciation, exemplifiedbytheincorporationofphotosyntheticunitsinseaslugs(Wa¨geleetal.), bytheroleofcuticularpropertiesinfungus-growingtermites(Martenetal.),andby thedifferentialpropertiesoftheelectricorganinAfricanfishespromotingecologi- cal speciation (Tiedemann et al.). With that, one of the major subjects of modern speciationstudiesisoncemoreemerging,viz.testingthecontributionofecological versusgeographicalfactors,asthenalsoinvestigatedinthepaperbySchubartetal. on the adaptive nature of a radiation of freshwater crabs on Jamaica. The three subsequentpaperslookmorespecificallyintothespatialcomponentofspeciation, usingasexemplarstheformerlyassumed“ringspecies”oftheLarusgullcomplex (Liebers-Helbigetal.),waterfrogsintheeasternMediterranean(Plo¨tneretal.),and hithertocrypticspeciesinCorsicanLimaxslugs(Nitzetal.).Inadditiontothelatter paper that also deals predominantly with reproductive characters and properties, twomorechaptersexaminetheroleofsexualselectioninspeciation,asillustrated forCretanlandsnailsbySauerandHausdorf,andbyMayeretal.foracoustically communicating grasshoppers, both in their way testing or providing evidence for non-ecologicalradiations.Thepossibilityofsympatricspeciationisfurtherexam- ined by Herder and Schliewen for lacustrine fishes in lakes on the Indonesian islands of Sulawesi. I am convinced that these central highland lakes provide us with a highly suitable “natural laboratory” for speciation studies, potentially even viii Preface bettersuitedthanotherancientlakesystems,inordertotestthedifferentialroleof allopatry versus sympatry, with a suite of geographical and ecological factors discernable, as shown for example in our own study of the endemic Tylomelania gastropods (Rintelen et al.). In the subsequent paper by Ko¨hler et al., we further examinethesethemesforanothercloselyrelatedlimnicsnailgroup;however,this timenotforalacustrinebutinsteadariverinesetting.Finally,thezoologicalsection is complemented by another study on limnic snails (a group of invertebrates obviously on its way of being recognized as an emerging model system in evolu- tionarybiology),withWilkeetal.investigating,thistimeexplicitly,thepossibility ofnon-adaptiveradiations. As is evident from the present compilation in this book, we are still far away frombeingabletoprovideabalancedviewonradiationandspeciation,asweare not even close to looking comprehensively at the major organisms, regions, or factorsinvolved.Whilesometaxaareexaminedhereinverythoroughly,othersare completelymissing.Nevertheless,wediscusssomeofthemostprominentfactors and highlight future avenues of research. In any case, I am convinced that these paperspresentedhereallshow,inavarietyofways,evolutioninaction. As authors of these papers as well as participants of the DFG priority programme, we are in great debt to the organisers, Klaus Bachmann and William Martin,whoprovidedamajortriggerforsynthesizingourwork.Wearegratefulfor thefinancialsupportbytheDFGandthecontinuoussupportbyitsrepresentative, RoswithaScho¨nwitz,aswellasgratefultothemembersofthereviewboardforthe many stimulating suggestions and discussions during these six exciting and suc- cessfulresearchyears,andtothereviewersofthe25paperspublishedherefortheir commentsandconstructivecriticisms. IwouldliketothankHaraldSchneiderwhohashelpedduringthereviewprocess with handling the botanical and host–plant interaction papers, Bill Martin for establishing contact with Springer, Heidelberg, and Sabine Schwarz and Anette Lindqvist of its Life Sciences Editorial Office for their encouragement and help throughouttheprocessofeditingthisvolume. Berlin MatthiasGlaubrecht February2010 Introduction to the Priority Programme “Radiations: Origins of Biological Diversity” This bookresultsfrom afocused researchprogramme,apriority programme,that was funded by the German Research Foundation (DFG) during the period 2002– 2007 entitled “Radiations: Origins of Biological Diversity” (priority programme SPP 1127). The programme was a landmark boost for studies in ecology and evolution at the species level in Central Europe, and it brought together a broad spectrumofevolutionarybiologists,unitedbyasinglepressingquestionaboutthe drivingforcesbehindspeciesdiversification. ThisisagoodopportunitytoansweraquestionthatIhaveoftenbeenasked:how did the programme SPP 1127 come to be? Adjunct to the annual meeting of the GermanBotanicalSocietyfor2000inJena,officersandrepresentativesoftheDFG invited a group of about 20 scientists from botany, zoology, microbiology, and ecologytoaone-daybrainstormingsessiononevolutionandsystematics,withthe goal of identifying some of the big outstanding questions in the field, efforts towards whose solution would generate substantial progress in our understanding ofbiodiversity.Italsohadtobesomethingharboringinterestandresearchpotential forthoseintheplant,animal,andmicrobialfields.Ourbrainsastorm,andwiththe flamesofdiscussionraging,wesearchedourgraymatterhouruponhourforissues genuinelyoriginal,scientificallyofoutstandingvalue,andatthesametimeofbroad enoughappealtoattracttheinterestsofchemistsandphysicists,forexample,soas to be of obvious significance beyond a specialist audience. Good ideas are cheap. We needed a great idea. By mid-afternoon, things started to look pretty bleak, as did many faces around the table, and we had got to the point where we were discussing with mostly genuine enthusiasm things like “The postglacial recoloni- zation of Europe”, which is no doubt of great interest, especially for those of us living in Central Europe, but maybe not the biggest evolutionary topic ever identified. Justwhenitseemedthattherewerenobigquestionsleftorotherwiseidentifiable inourstorm-sweptmindsaboutspecies-levelevolution,thewatersparted.Oneof the world’s leading botanists, Friedrich Ehrendorfer, opened up the afternoon sessionwiththememorablyboomingwords“Radiations!Ifwewanttounderstand ix